Developmental time windows for axon growth influence neuronal network topology
详细信息    查看全文
  • 作者:Sol Lim (1) (2)
    Marcus Kaiser (1) (2) (3)

    1. Department of Brain and Cognitive Sciences
    ; Seoul National University ; Seoul ; Republic of Korea
    2. Interdisciplinary Computing and Complex BioSystems Group (ICOS)
    ; School of Computing Science ; Newcastle University ; Claremont Tower ; Newcastle upon Tyne ; NE1 7RU ; UK
    3. Institute of Neuroscience
    ; Newcastle University ; Newcastle upon Tyne ; UK
  • 关键词:Brain connectivity ; Network development ; Computational neuroanatomy ; Complex networks ; Neural networks
  • 刊名:Biological Cybernetics
  • 出版年:2015
  • 出版时间:April 2015
  • 年:2015
  • 卷:109
  • 期:2
  • 页码:275-286
  • 全文大小:1,366 KB
  • 参考文献:1. Andersen, SL (2003) Trajectories of brain development: point of vulnerability or window of opportunity?. Neurosci Biobehav Rev 27: pp. 3-18 CrossRef
    2. Baruch, L, Itzkovitz, S, Golan-Mashiach, M, Shapiro, E, Segal, E (2008) Using expression profiles of Caenorhabditis elegans neurons to identify genes that mediate synaptic connectivity. PLoS Comput Biol 4: pp. e1000120 CrossRef
    3. Binzegger, T, Douglas, RJ, Martin, KAC (2004) A quantitative map of the circuit of cat primary visual cortex. J Neurosci 24: pp. 8441-8453 CrossRef
    4. Braitenberg, V, Sch眉z, A (1998) Cortex: statistics and geometry of neuronal connectivity. Springer, Heidelberg CrossRef
    5. Brandes, U, Erlebach, T (2005) Network analysis. Lecture Notes in Computer Science. Springer, Heidelberg
    6. Butz, M, Steenbuck, ID, Ooyen, A (2014) Homeostatic structural plasticity increases the efficiency of small-world networks. Front Synaptic Neurosci 6: pp. 7 CrossRef
    7. Butz, M, Ooyen, A (2013) A simple rule for dendritic spine and axonal bouton formation can account for cortical reorganization after focal retinal lesions. PLoS Comput Biol 9: pp. e1003259 CrossRef
    8. Butz, M, W枚rg枚tter, F, Ooyen, A (2009) Activity-dependent structural plasticity. Brain Res Rev 60: pp. 287-305 CrossRef
    9. Chen, BL, Hall, DH, Chklovskii, DB (2006) Wiring optimization can relate neuronal structure and function. Proc Natl Acad Sci USA 103: pp. 4723-4728 CrossRef
    10. Choe Y, McCormick B, Koh W (2004) Network connectivity analysis on the temporally augmented / C. elegans web: a pilot study. In: Society for neuroscience abstracts, vol 921.9
    11. Costa, LdF, Rodrigues, FA, Travieso, G (2007) Characterization of complex networks: a survey of measurements. Adv Phys 56: pp. 167-242 CrossRef
    12. Deguchi, Y, Donato, F, Galimberti, I, Cabuy, E, Caroni, P (2011) Temporally matched subpopulations of selectively interconnected principal neurons in the hippocampus. Nat Neurosci 14: pp. 495-504 CrossRef
    13. Dickson, B (2002) Molecular mechanisms of axon guidance. Science 298: pp. 1959-1964 CrossRef
    14. Dickson, BJ (2002) Molecular mechanisms of axon guidance. Science 298: pp. 1959-1964 CrossRef
    15. Druckmann, S, Feng, L, Lee, B, Yook, C, Zhao, T, Magee, JC, Kim, J (2014) Structured synaptic connectivity between hippocampal regions. Neuron 81: pp. 629-640 CrossRef
    16. Easter, SS, Purves, D, Rakic, P, Spitzer, NC (1985) The changing view of neural specificity. Science 230: pp. 507-511 CrossRef
    17. Franze, K (2013) The mechanical control of nervous system development. Development 140: pp. 3069-3077 CrossRef
    18. Godfrey, KB, Eglen, SJ, Swindale, NV (2009) A multi-component model of the developing retinocollicular pathway incorporating axonal and synaptic growth. PLoS Comput Biol 5: pp. e1000600 CrossRef
    19. Gotz, M, Novak, N, Bastmeyer, M, Bolz, J (1992) Membrane-bound molecules in rat cerebral cortex regulate thalamic innervation. Development 116: pp. 507-519
    20. Hall, DH, Altun, ZF (2008) C. elegans atlas. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
    21. Hellwig, B (2000) A quantitative analysis of the local connectivity between pyramidal neurons in layers 2/3 of the rat visual cortex. Biol Cybern 82: pp. 111-121 CrossRef
    22. Hennig, MH, Adams, C, Willshaw, D, Sernagor, E (2009) Early-stage waves in the retinal network emerge close to a critical state transition between local and global functional connectivity. J Neurosci 29: pp. 1077-1086 CrossRef
    23. Hill, SL, Wang, Y, Riachi, I, Sch眉rmann, F, Markram, H (2012) Statistical connectivity provides a sufficient foundation for specific functional connectivity in neocortical neural microcircuits. Proc Nat Acad Sci 109: pp. E2885-E2894 CrossRef
    24. Huttenlocher, P (1984) Synapse elimination and plasticity in developing human cerebral cortex. Am J Mental Defic 88: pp. 488-496
    25. Kaiser, M (2011) A tutorial in connectome analysis: topological and spatial features of brain networks. Neuroimage 57: pp. 892-907 CrossRef
    26. Kaiser, M, Hilgetag, CC (2006) Nonoptimal component placement, but short processing paths, due to long-distance projections in neural systems. PLoS Comput Biol 2: pp. e95 CrossRef
    27. Kaiser, M, Hilgetag, CC (2007) Development of multi-cluster cortical networks by time windows for spatial growth. Neurocomputing 70: pp. 1829-1832 CrossRef
    28. Kaiser, M, Hilgetag, CC, Ooyen, A (2009) A simple rule for axon outgrowth and synaptic competition generates realistic connection lengths and filling fractions. Cereb Cortex 19: pp. 3001-3010 CrossRef
    29. Kaiser, M, Varier, S (2011) Evolution and development of brain networks: from Caenorhabditis elegans to Homo sapiens. Netw Comput Neural Syst 22: pp. 143-147
    30. Kaufman, A, Dror, G, Meilijson, I, Ruppin, E (2006) Gene expression of C. elegans neurons carries information on their synaptic connectivity. PLoS Comput Biol 2: pp. e167 CrossRef
    31. Kelsch, W, Sim, S, Lois, C (2010) Watching synaptogenesis in the adult brain. Annu Rev Neurosci 33: pp. 131-149 CrossRef
    32. Koene, RA, Tijms, B, Hees, P, Postma, F, Ridder, A, Ramakers, GJ, Pelt, J, Ooyen, A (2009) NETMORPH: a framework for the stochastic generation of large scale neuronal networks with realistic neuron morphologies. Neuroinformatics 7: pp. 195-210 CrossRef
    33. Krottje, JK, Ooyen, A (2007) A mathematical framework for modelling axon guidance. Bull Math Biol 69: pp. 3-31 CrossRef
    34. Latora, V, Marchiori, M (2001) Efficient behavior of small-world networks. Phys Rev Lett 87: pp. 198701 CrossRef
    35. Latora, V, Marchiori, M (2003) Economic small-world behavior in weighted networks. Eur Physl J B Condens Matter Complex Syst 32: pp. 249-263 CrossRef
    36. Li, W-C, Cooke, T, Sautois, B, Soffe, S, Borisyuk, R, Roberts, A (2007) Axon and dendrite geography predict the specificity of synaptic connections in a functioning spinal cord network. Neural Dev 2: pp. 17 CrossRef
    37. Li, Y, Liu, Y, Li, J, Qin, W, Li, K, Yu, C, Jiang, T (2009) Brain anatomical network and intelligence. PLoS Comput Biol 5: pp. e1000395 CrossRef
    38. Markram, H, L眉bke, J, Frotscher, M, Roth, A, Sakmann, B (1997) Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. J Physiol 500: pp. 409-440 CrossRef
    39. Maslov, S, Sneppen, K (2002) Specificity and stability in topology of protein networks. Science 296: pp. 910-913 CrossRef
    40. McAssey, MP, Bijma, F, Tarigan, B, Pelt, J, Ooyen, A, Gunst, M (2014) A morpho-density approach to estimating neural connectivity. PLOS One 9: pp. e86526 CrossRef
    41. Newman, MEJ (2003) The structure and function of complex networks. SIAM Rev 45: pp. 167-256 CrossRef
    42. Nisbach, F, Kaiser, M (2007) Developmental time windows for spatial growth generate multiple-cluster small-world networks. Eur Phys J B 58: pp. 185-191 CrossRef
    43. Packer, AM, McConnell, DJ, Fino, E, Yuste, R (2013) Axo-dendritic overlap and laminar projection can explain interneuron connectivity to pyramidal cells. Cereb Cortex 23: pp. 2790-2802 CrossRef
    44. Packer, AM, Yuste, R (2011) Dense, unspecific connectivity of neocortical parvalbumin-positive interneurons: a canonical microcircuit for inhibition?. J Neurosci 31: pp. 13260-13271 CrossRef
    45. Perin, R, Berger, TK, Markram, H (2011) A synaptic organizing principle for cortical neuronal groups. Proc Nat Acad Sci 108: pp. 5419-5424 CrossRef
    46. Perin, R, Telefont, M, Markram, H (2013) Computing the size and number of neuronal clusters in local circuits. Front Neuroanat 7: pp. 1 CrossRef
    47. Price, D, Jarman, AP, Mason, JO, Kind, PC (2011) Building brains, an introduction to neural development. Wiley, New York CrossRef
    48. Purves, D, Lichtman, JW (1980) Elimination of synapses in the developing nervous system. Science 210: pp. 153-157 CrossRef
    49. Rakic, P (2002) Neurogenesis in adult primate neocortex: an evaluation of the evidence. Nat Rev Neurosci 3: pp. 65-71 CrossRef
    50. Rakic, P, Bourgeois, JP, Eckenhoff, MF, Zecevic, N, Goldman-Rakic, PS (1986) Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex. Science 232: pp. 232-235 CrossRef
    51. Ropireddy, D, Ascoli, GA (2011) Potential synaptic connectivity of different neurons onto pyramidal cells in a 3D reconstruction of the rat hippocampus. Front Neuroinform 5: pp. 5 CrossRef
    52. Rubinov, M, Sporns, O (2010) Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52: pp. 1059-1069 CrossRef
    53. Sakai, N, Kaprielian, Z (2012) Guidance of longitudinally projecting axons in the developing central nervous system. Front Mol Neurosci 5: pp. 59 CrossRef
    54. Samsonovich, AV, Ascoli, GA (2003) Statistical morphological analysis of hippocampal principal neurons indicates cell-specific repulsion of dendrites from their own cell. J Neurosci Res 71: pp. 173-187 CrossRef
    55. Scheiffele, P, Fan, J, Choih, J, Fetter, R, Serafini, T (2000) Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 101: pp. 657-669 CrossRef
    56. Schuz, A (2005) Quantitative aspects of corticocortical connections: a tracer study in the mouse. Cereb Cortex 16: pp. 1474-1486 CrossRef
    57. Shaw, P, Kabani, NJ, Lerch, JP, Eckstrand, K, Lenroot, R, Gogtay, N, Greenstein, D, Clasen, L, Evans, A, Rapoport, JL (2008) Neurodevelopmental trajectories of the human cerebral cortex. J Neurosci 28: pp. 3586-3594 CrossRef
    58. Sperry, RW (1963) Chemoaffinity in the orderly growth of nerve fiber pattern and connections. Proc Natl Acad Sci USA 50: pp. 703-710 CrossRef
    59. Stepanyants, A, Hof, PR, Chklovskii, DB (2002) Geometry and structural plasticity of synaptic connectivity. Neuron 34: pp. 275-288 CrossRef
    60. Sur, M, Leamey, CA (2001) Development and plasticity of cortical areas and networks. Nat Rev Neurosci 2: pp. 251-262 CrossRef
    61. Ooyen, A (2001) Competition in the development of nerve connections: a review of models. Netw Comput Neural Syst 12: pp. 1-47 CrossRef
    62. Ooyen, A (2003) Modeling neural development. MIT Press, Cambridge
    63. van Ooyen A (2011) Using theoretical models to analyse neural development. Nat Rev Neurosci 12(6):311鈥?26
    64. van Ooyen A, Carnell A, de Ridder S, Tarigan B, Mansvelder HD, Bijma F, de Gunst M, van Pelt J (2014) Independently outgrowing neurons and geometry-based synapse formation produce networks with realistic synaptic connectivity. PLoS One 9(1):e85858
    65. Ooyen, AP, Graham, BJA, Ramakers, G (2001) Competition for tubulin between growing neurites during development. Neurocomputing 38鈥?0: pp. 73-78 CrossRef
    66. Ooyen, A, Pelt, J, Corner, MA (1995) Implications of activity dependent neurite outgrowth for neuronal morphology and network development. J Theor Biol 172: pp. 63-82 CrossRef
    67. Pelt, J, Ooyen, A (2013) Estimating neuronal connectivity from axonal and dendritic density fields. Front Comput Neurosci 7: pp. 160
    68. Varier, S, Kaiser, M (2011) Neural development features: spatio-temporal development of the Caenorhabditis elegans neuronal network. PLoS Comput Biol 7: pp. e1001044 CrossRef
    69. Varshney, LR, Chen, BL, Paniagua, E, Hall, DH, Chklovskii, DB (2011) Structural properties of the Caenorhabditis elegans neuronal network. PLoS Comput Biol 7: pp. e1001066 CrossRef
    70. Verhage, M, Maia, AS, Plomp, JJ, Brussaard, AB, Heeroma, JH, Vermeer, H, Toonen, RF, Hammer, RE, Berg, TK, Missler, M, Geuze, HJ, Sudhof, TC (2000) Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 287: pp. 864-869 CrossRef
    71. Willshaw, DJ, Malsburg, C (1976) How patterned neural connections can be set up by self-organization. Proc R Soc Lond Ser B Contain Pap Biol Character 194: pp. 431-445 CrossRef
    72. Yamamoto, N, Tamada, A, Murakami, F (2002) Wiring of the brain by a range of guidance cues. Prog Neurobiol 68: pp. 393-407 CrossRef
    73. Yu, Y-C, Bultje, RS, Wang, X, Shi, S-H (2009) Specific synapses develop preferentially among sister excitatory neurons in the neocortex. Nature 458: pp. 501-504 CrossRef
    74. Yu, Y-C, He, S, Chen, S, Fu, Y, Brown, KN, Yao, X-H, Ma, J, Gao, KP, Sosinsky, GE, Huang, K (2012) Preferential electrical coupling regulates neocortical lineage-dependent microcircuit assembly. Nature 486: pp. 113-117
    75. Zawadzki, K, Feenders, C, Viana, MP, Kaiser, M (2012) Morphological homogeneity of neurons: searching for outlier neuronal cells. Neuroinformatics 10: pp. 379-389 CrossRef
    76. Zubler, F, Douglas, R (2009) A framework for modeling the growth and development of neurons and networks. Front Comput Neurosci 3: pp. 25 CrossRef
  • 刊物类别:Biomedical and Life Sciences
  • 刊物主题:Biomedicine
    Neurosciences
    Computer Application in Life Sciences
    Neurobiology
    Bioinformatics
  • 出版者:Springer Berlin / Heidelberg
  • ISSN:1432-0770
文摘
Early brain connectivity development consists of multiple stages: birth of neurons, their migration and the subsequent growth of axons and dendrites. Each stage occurs within a certain period of time depending on types of neurons and cortical layers. Forming synapses between neurons either by growing axons starting at similar times for all neurons (much-overlapped time windows) or at different time points (less-overlapped) may affect the topological and spatial properties of neuronal networks. Here, we explore the extreme cases of axon formation during early development, either starting at the same time for all neurons (parallel, i.e., maximally overlapped time windows) or occurring for each neuron separately one neuron after another (serial, i.e., no overlaps in time windows). For both cases, the number of potential and established synapses remained comparable. Topological and spatial properties, however, differed: Neurons that started axon growth early on in serial growth achieved higher out-degrees, higher local efficiency and longer axon lengths while neurons demonstrated more homogeneous connectivity patterns for parallel growth. Second, connection probability decreased more rapidly with distance between neurons for parallel growth than for serial growth. Third, bidirectional connections were more numerous for parallel growth. Finally, we tested our predictions with C. elegans data. Together, this indicates that time windows for axon growth influence the topological and spatial properties of neuronal networks opening up the possibility to a posteriori estimate developmental mechanisms based on network properties of a developed network.

© 2004-2018 中国地质图书馆版权所有 京ICP备05064691号 京公网安备11010802017129号

地址:北京市海淀区学院路29号 邮编:100083

电话:办公室:(+86 10)66554848;文献借阅、咨询服务、科技查新:66554700